A previous study predicted the evolution of monogamy in symbiotic crustaceans inhabiting scarce, relatively small hosts in tropical environments where predation risk away from hosts is high. This prediction was tested in the shrimp Pontonia margarita, which inhabits the pearl oyster Pinctada mazatlanica. A total of 68 oysters were collected from the intertidal and shallow subtidal at two islands (Islas Secas [N 27° 55′, W 82° 03′] and Isla de La Coiba [N 27° 50′, W 97° 03′]) off the eastern tropical Pacific coast on 15 and 17 March 2007, respectively. The population structure, distribution, male-female association pattern, and relative growth of the major claw and pleura of the second abdominal segment of each shrimp retrieved were examined. Shrimps were found as heterosexual pairs in the mantle cavity of hosts more frequently than would be expected by chance alone. Males occurred with females in the same host, independent of the reproductive condition of the female or the stage of development of brooded embryos. This observation, and strong correlations between the host and shrimp body size in both males and females suggest a long-term association between males and females in each host. Sexual dimorphism in body size was minor, with males being just slightly smaller than females. In agreement with predictions for monogamous species, the major claw of males did not display positive allometry, which has been generally reported for polygamous shrimps. In turn, the pleura of the second abdomen presented negative allometry in males but positive allometry in females. All available information suggests that Pontonia margarita has a socially monogamous mating system with males and females forming exclusive pairs in their hosts.